Journal of General Virology (1993), 74, 985-994. Printedin Great Britain 985
Neurons containing latency-associated transcripts are numerous and
widespread in dorsal root ganglia following footpad inoculation of mice
with herpes simplex virus type 1 mutant in1814
M. S. Ecob-Prince, ~* C. M. Preston, z F. J. Rixon, z K. Hassan ~ and P. G. E. Kennedy ~
1Department of Neurology, University of Glasgow, Institute of Neurological Sciences, Southern General Hospital,
Glasgow G51 4TF and 2MRC Virology Unit, Church Street, Glasgow Gll 5JR, U.K.
The herpes simplex virus type 1 (HSV-1) mutant in1814
lacks the ability to trans-activate immediate early gene
transcription and enter lytic replication but it can
establish and reactivate from latency. We therefore
investigated the number of neurons that expressed
latency-associated transcripts (LATs) in animals latently
infected with in1814, the rescued revertant (1814R), or
wild-type (wt) HSV-1. The percentage of LAT + neurons
increased with increasing doses of each of the viruses.
After inoculation of equal amounts of infectious virus
many more LAT + neurons were observed in animals
infected with in1814 than with 1814R or wt HSV-1.
Whereas the LAT + neurons in animals infected with
1814R or wt HSV-1 were largely confined to lumbar
dorsal root ganglia (DRG) L4/L5/L6 (those which
innervate the lower leg), in animals infected with in1814
they were also present in DRG not directly involved with
such innervation (thoracic 12 and 13, L1, L2 and L3).
We concluded that the large number of LAT + neurons
observed with in1814 was related to the high particle
numbers in the inoculum and that spread of virus was
related to limited replication as well as to the low
neurovirulence of in1814. This spread was not unique to
in1814 but when it occurred with more virulent viruses
such as 1814R or wt HSV-1, it resulted in the death of
the host.
Introduction
When herpes simplex virus (HSV) is inoculated intrader-
mally into a mouse it establishes a latent infection in the
sensory neurons of the ganglia that innervate the
dermatome (Stevens & Cook, 1971). In the case of the
footpad this is mainly the dorsal root ganglia (DRG) of
lumbar segment 5 (L5), with some contribution also
from L4 and L6 (Greene, 1959). Although latent viral
DNA can be found in the relevant ganglia (Efstathiou et
al., 1986; Katz et al., 1990), it cannot be detected on an
individual cell basis by in situ hybridization for reasons
that are not yet understood (Stevens, 1989). However,
there is limited transcription of the HSV genome during
latency and latency-associated transcripts (LATs) ac-
cumulate in the nucleus of neurons in mice (Deatly et al.,
1987; Spivack & Fraser, 1987; Stevens et al., 1987),
rabbits (Rock et al., 1987; Wagner et al., 1988) and
humans (Croen et al., 1987; Gordon et al., 1988;
Wechsler et al., 1988) where they can be detected by in
situ hybridization. The major LAT is a 2-0 kb RNA
which may be an intron spliced from an 8-3 kb transcript
(Farrell et al., 1991) or an alterative transcription unit
using the same promoter as the 8.3 kb mRNA (Spivack
et al., 1991). The function of LATs remains unclear but
viruses from which the LAT gene has been deleted can
establish, maintain and reactivate from latent infections
(Javier et al., 1988; Ho & Mocarski, 1989; Steiner et al.,
1989; Izumi et al., 1989; Block et al., 1990), although
reactivation in some cases is delayed or less efficient (Leib
e t al., 1989 a; Hill et al., 1990; Trousdale et al., 1991).This
reduced reactivation may, however, be the result of fewer
latently infected cells in the DRG from which re-
activation can take place, supporting the idea that LATs
have a role in the efficient establishment of latent
infections (Sawtell & Thompson, 1992). Nevertheless,
the presence of LATs in a cell is thought to be a marker
of latent virus infection.
The percentage of neurons in which a latent infection
becomes established is very low. Detection of viral
nucleic acid suggests that between 1% and 5 % of the
neurons are involved (Galloway et al., 1979; Stevens,
1989; Speck & Simmons, 1991 ; Rock et al., 1992). How-
ever, when DRG were serially sectioned to quantify
LAT + cells, only 24 (0.65 %) were found in 3500 neurons
of the L5 ganglion (Tenser et al., 1989). We therefore
investigated whether a mutant of HSV, which was less
able than wild-type (wt) HSV to enter a lytic replication
cycle, would establish larger numbers of LAT + neurons.
The mutant in1814 (Ace et al., 1989) has a 12 bp
0001-1350 © 1993 SGM